diff --git a/apps/web/src/components/chat/ModelPickerContent.tsx b/apps/web/src/components/chat/ModelPickerContent.tsx
index 73fc2c94b1e7a..efeacbd4b3cd5 100644
--- a/apps/web/src/components/chat/ModelPickerContent.tsx
+++ b/apps/web/src/components/chat/ModelPickerContent.tsx
@@ -163,6 +163,11 @@ function adjacentModelPickerProvider(input: {
 
 const EMPTY_MODEL_JUMP_LABELS = new Map<string, string>();
 const MODEL_LIST_ESTIMATED_ITEM_SIZE = 52;
+// Rendered heights in `--spacing` units. Chrome is the search box and list padding, plus a 1px border.
+const ONE_LINE_ROW_UNITS = 8;
+const TWO_LINE_ROW_UNITS = { classic: 11.25, redesign: 12 };
+const ROW_SEPARATOR_UNITS = 0.5;
+const LIST_CHROME_UNITS = 15.5;
 
 function ModelListSeparator() {
   return <div className="h-0.5" />;
@@ -259,10 +264,6 @@ function ModelPickerList({
 }) {
   const [showTopScrollFade, setShowTopScrollFade] = useState(false);
   const [showBottomScrollFade, setShowBottomScrollFade] = useState(false);
-  const [contentSize, setContentSize] = useState(
-    () => itemKeys.length * MODEL_LIST_ESTIMATED_ITEM_SIZE,
-  );
-  useLayoutEffect(() => listRef.current?.getState().listen("totalSize", setContentSize), [listRef]);
   const updateScrollFades = () => {
     const scrollElement = listRef.current?.getScrollableNode();
     if (!(scrollElement instanceof HTMLElement)) {
@@ -297,10 +298,10 @@ function ModelPickerList({
 
   return (
     <div
-      className="relative min-h-0 overflow-hidden pr-px"
-      style={{
-        height: itemKeys.length === 0 ? 0 : `calc(${contentSize}px + var(--spacing) * 5)`,
-      }}
+      className={cn(
+        "relative min-h-0 overflow-hidden pr-px",
+        itemKeys.length > 0 ? "flex-1" : "h-0",
+      )}
     >
       <ComboboxListVirtualized>
         <LegendList<string>
@@ -578,6 +579,33 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
   // Inside one provider's tab the provider line repeats the selected rail icon on every row.
   const redesign = useClientSettings((s) => s.redesignEnabled);
   const rowsMixProviders = !redesign || isSearching || selectedInstanceId === "favorites";
+  // Fit the tallest tab so switching tabs never resizes the popup and moves the rail under the cursor.
+  const tallestTabUnits = (() => {
+    const unitsByTab = new Map<ProviderInstanceId | "favorites", number>();
+    const addRow = (tab: ProviderInstanceId | "favorites", twoLine: boolean) => {
+      const rowUnits = twoLine
+        ? TWO_LINE_ROW_UNITS[redesign ? "redesign" : "classic"]
+        : ONE_LINE_ROW_UNITS;
+      const previous = unitsByTab.get(tab);
+      unitsByTab.set(
+        tab,
+        previous === undefined ? rowUnits : previous + ROW_SEPARATOR_UNITS + rowUnits,
+      );
+    };
+    const tabsWithLegacyRow = new Set<ProviderInstanceId>();
+    for (const model of flatModels) {
+      if (!matchesLockedProvider(model)) continue;
+      const isFavorite = favoritesSet.has(providerModelKey(model.instanceId, model.slug));
+      if (isFavorite) addRow("favorites", true);
+      if (model.isLegacy && !isFavorite) {
+        tabsWithLegacyRow.add(model.instanceId);
+      } else {
+        addRow(model.instanceId, !redesign || Boolean(model.subProvider));
+      }
+    }
+    for (const instanceId of tabsWithLegacyRow) addRow(instanceId, true);
+    return Math.max(0, ...unitsByTab.values());
+  })();
   const lockedDisabledInstanceIds = (() => {
     if (!isLocked) {
       return undefined;
@@ -799,7 +827,13 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
       <div
         ref={pickerContentRef}
         className="relative flex max-h-86.5 w-screen max-w-90 flex-row overflow-hidden"
-        style={isSearching ? { height: searchHeight } : undefined}
+        style={
+          isSearching
+            ? { height: searchHeight }
+            : {
+                minHeight: `min(calc(var(--spacing) * ${tallestTabUnits + LIST_CHROME_UNITS} + 1px), calc(var(--spacing) * 86.5))`,
+              }
+        }
         data-model-picker-content="true"
       >
         {showSidebar && (